Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience

By Jadin C. Jackson, Adam Johnson, A. David Redish. 2006

142 citations recorded by the source corpus.

Hippocampal firing patterns during behavior are reactivated during rest and subsequent slow-wave sleep. These reactivations occur during transient local field potential (LFP) events, termed sharp waves. Theories of hippocampal processing suggest that sharp waves arise from strengthened plasticity, and that the strengthened plasticity depends on repeated cofiring of pyramidal cells. We tested these predictions by recording neural ensembles and LFPs from rats running tasks requiring different levels of behavioral repetition. The number of sharp waves emitted increased during sessions with more regular behaviors. Reactivation became more similar to behavioral firing patterns across the session. This enhanced reactivation also depended on the regularity of the behavior. Additional studies in CA3 and CA1 found that the number of sharp waves emitted also increased in CA3 recordings as well as CA1, but that the time courses were different between the two structures.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, background): “Examination of the similarity of pairwise neural co-firing during awake SWRs and during awake exploration first suggested that activity during awake SWRs can reactivate past, rather than current, experience”
Hippocampal Replay is Not a Simple Function of Experience (2010, methodology): “Whereas previous studies (Wil- son and McNaughton, 1994; Jackson et al., 2006; O’Neill et al., 2006; Karlsson and Frank, 2009) have found increasing replay with experience, these studies did not compare tasks with different behavioral requirements in which parts of the environment were experienced…”
Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration (2007, background): “SWR patterns are present not only during slow wave sleep, but also during periods of waking immobility, consummatory behaviour and grooming (Buzsaki et al., 1983; Buzsaki, 1989; Foster & Wilson, 2006; Jackson et al., 2006; O’Neill et al., 2006).”
The content of hippocampal “replay” (2018, background): “, 1983), and initial pairwise correlation studies indicated that awake ripples may also replay experience-relevant sequences (Jackson et al., 2006; Kudrimoti et al., 1999; O’Neill et al., 2006).”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “The robust nature of the reverse replay of place cell sequences was immediately replicated in other laboratories in both CA1 and CA3 regions (Jackson et al., 2006; Csicsvari et al., 2007; Diba and Buzs aki, 2007).”
Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point (2007, background): “Local field potentials Extrafield firing has been known to occur during sharp-wave ripple complexes within LIA episodes (O’Keefe and Nadel, 1978; Kudrimoti et al., 1999; Jensen and Lisman, 2000; Foster and Wilson, 2006; Jackson et al., 2006; O’Neill et al., 2006).”
Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility (2017, unknown): “…activity patterns correspond to representations of trajectories through space (Csicsvari et al., 2007; Davidson et al., 2009; Diba and Buzsáki, 2007; Foster and Wilson, 2006; Gupta et al., 2010; Jackson et al., 2006; Karlsson and Frank, 2009; Pfeiffer and Foster, 2013; Wu and Foster, 2014).”
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus (2009, unknown): “We also calculated behavioral entropy as described previously (Jackson et al., 2006) so that we could identify any differences in behavior between rewarded and unrewarded trials (see Supplementary Experimental Procedures and Supplemental Results).”
Hippocampus Leads Ventral Striatum in Replay of Place-Reward Information (2009, background): “Alternatively, the same result may be explained by an enhancement of reactivation detectability along with task familiarity [4].”
The Role of Hippocampal Replay in Memory and Planning (2018, background): “often representing non-local positions [48,57,63,64] de-coupled from the animal’s future path [121].”
New experiences enhance coordinated neural activity in the hippocampus. (2008, unknown): “Neurons with overlapping place fields tend to fire together when the animal is located outside the place fields during later periods of sleep (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Kudrimoti et al., 1999; Louie and Wilson, 2001; Le”